LONG-TERM NETWORK EXCITABILITY IN THE HIPPOCAMPUS: LINKING SOCIAL-TERRITORIAL LEARNING, AGGRESSION, AND CIRCUIT DYNAMICS

Territoriality is a social behavior where individuals establish and defend a spatial domain against conspecifics, yet its neural underpinnings remain poorly understood. We hypothesized that territorial aggression emerges from neural circuits integrating spatial and mnemonic information, with a central role for the hippocampal dentate gyrus (DG). We examined population-level dynamics in the dorsal DG observing development of territorial behavior using a resident–intruder paradigm with in vivo calcium imaging using a head-mounted Miniscope. Male ICR mice expressing a genetically encoded calcium indicator in the dorsal DG were housed with a sterile female for 21 days to establish territorial ownership. Beginning on day 21, residents were exposed daily to a male intruder. During early encounters, residents exhibited predominantly social, non-aggressive behavior, accompanied by sparse and stable DG activity. After typically 3 to 5 days a marked transition occurred, and mice displayed robust aggression alongside a striking increase in DG activity, termed Long-Term Network Excitability (LTNE). LTNE involved a three- to tenfold rise in the number of active DG neurons, coinciding with the behavioral shift to aggression. Most newly recruited neurons exhibited spatial tuning characteristic of place cells, which remained stable across sessions and contexts. This indicates that territorial aggression is associated with large-scale, structured reorganization of spatially encoded DG ensembles rather than nonspecific activation. Notably, aggressive behavior persisted even after DG activity partially subsided, suggesting that transient network excitability triggers enduring behavioral change. These findings demonstrate that repeated territorial challenge induces profound, experience-dependent plasticity in the dentate gyrus.